Retrieval facilitates the long-term retention of memories, but may also enable stored representat... more Retrieval facilitates the long-term retention of memories, but may also enable stored representations to be updated with new information that is available at the time of retrieval. However, if information integrated during retrieval is erroneous, future recall can be impaired: a phenomenon known as retrieval-induced distortion (RID). Whether RID causes an " overwriting " of existing memory traces or leads to the coexistence of original and distorted memory traces is unknown. Because sleep enhances memory consolidation, the effects of sleep after RID can provide novel insights into the structure of updated memories. As such, we investigated the effects of sleep on memory consolidation following RID. Participants encoded word locations and were then tested before (T1) and after (T2) an interval of sleep or wakefulness. At T2, the majority of words were placed closer to the locations retrieved at T1 than to the studied locations, consistent with RID. After sleep compared with after wake, the T2-retrieved locations were closer to both the studied locations and the T1-retrieved locations. These findings suggest that RID leads to the formation of an additional memory trace that corresponds to a distorted variant of the same encoding event, which is strengthened alongside the original trace during sleep. More broadly, these data provide evidence for the importance of sleep in the preservation and adaptive updating of memories.
Study Objectives: Memories are strengthened during sleep. The benefits of sleep for memory can be... more Study Objectives: Memories are strengthened during sleep. The benefits of sleep for memory can be enhanced by re-exposing the sleeping brain to auditory cues; a technique known as targeted memory reactivation (TMR). Prior studies have not assessed the nature of the retrieval mechanisms underpinning TMR: the matching process between auditory stimuli encountered during sleep and previously encoded memories. We carried out two experiments to address this issue. Methods: In Experiment 1, participants associated words with verbal and nonverbal auditory stimuli before an overnight interval in which subsets of these stimuli were replayed in slow-wave sleep. We repeated this paradigm in Experiment 2 with the single difference that the gender of the verbal auditory stimuli was switched between learning and sleep. Results: In Experiment 1, forgetting of cued (vs. noncued) associations was reduced by TMR with verbal and nonverbal cues to similar extents. In Experiment 2, TMR with identical nonverbal cues reduced forgetting of cued (vs. noncued) associations, replicating Experiment 1. However, TMR with nonidentical verbal cues reduced forgetting of both cued and noncued associations. Conclusions: These experiments suggest that the memory effects of TMR are influenced by the acoustic overlap between stimuli delivered at training and sleep. Our findings hint at the existence of two processing routes for memory retrieval during sleep. Whereas TMR with acoustically identical cues may reactivate individual associations via simple episodic matching, TMR with nonidentical verbal cues may utilize linguistic decoding mechanisms, resulting in widespread reactivation across a broad category of memories.
Recent work has suggested that the benefits of sleep for memory consolidation are enhanced for hi... more Recent work has suggested that the benefits of sleep for memory consolidation are enhanced for highly salient (versus non-salient) memories. Using a technique known as targeted memory reactivation, it is possible to selectively strengthen newly learned memories by re-exposing the sleeping brain to auditory cues. The aim of the current study was to examine whether emotionally salient memories are also more responsive to targeted memory reactivation in slow-wave sleep than neutral memories. In an initial training phase, participants memorised emotionally negative and neutral pictures, which were each paired with a semantically related sound. Recognition for the pictures was assessed before and after a 90-min nap opportunity, during which half the sounds were represented during slow-wave sleep (as assessed via online polysomnographic sleep monitoring). We observed no effect of targeted memory reactivation on the recognition of emotionally negative or neutral memories. Our results highlight the importance of the memory paradigm used to assess targeted memory reactivation, and suggest that the robust and durable nature of recognition memory may make it an insensitive measure of behavioural targeted memory reactivation benefits. To fully assess the impacts of targeted memory reactivation on emotional memory processing in sleep, future studies should adopt experimental paradigms that maximise the salience of emotional stimuli while also providing a sensitive index of memory accuracy.
New memories are rarely formed as individual representations, but are stored in the context of co... more New memories are rarely formed as individual representations, but are stored in the context of cognitive schemas: mental frameworks within which we can organize and interpret related information (Bartlett, 1932). At school, for example, we acquire basic knowledge about the locations of different countries. This geographical schema then assists us later in life when learning about new countries, their locations, and cultural similarities. As our global knowledge grows, the learning and integration of new geographical information becomes increasingly efficient, and we can make inferences regarding the world around us. Schematic influences on learning can be understood in the context of dual systems models of memory (e.g., van Kesteren et al., 2012; McClelland, 2013). These models propose that new information is rapidly encoded by hippocampal networks, but becomes gradually integrated into the neocortex for long-term storage. However, where this new information is related to a schema, it benefits from existing neural connections and can thus be integrated more efficiently than unrelated information. Several recent studies have examined the neural mechanisms underlying schematic learning by generating artificial schema in the laboratory (e.g., Hennies et al., 2016). While informative and well-controlled, this method is unable to address how we utilize real-world knowledge that is not bound to the context of an experiment. Understanding whether the neural mechanisms underpinning schema-based learning are similar in relation to natural variations in existing knowledge remains a key research question. Gaining insights into the automaticity with which we can capitalize upon our existing knowledge in different settings from which it is acquired may have important implications for education. In a recent study, Brod et al. (2016) capitalized upon the advancing knowledge of medical students to gain more naturalistic insights into the neural basis of schema-relevant learning. While undergoing fMRI, participants learned a series of faces paired with either names or medical diagnoses (low or high relevance to medical knowledge, respectively). Immediately afterwards, outside of the scanner, they were represented with each face and asked to identify the associated name/diagnosis. This procedure enabled Brod et al. to identify patterns of neural activity at learning that predicted successful memory retrieval at test. Furthermore, this procedure was carried out with novel pairs both before and after 3 months of study for a medical exam, providing a measurable
Lexical competition is a hallmark of proficient, automatic word recognition. Previous research su... more Lexical competition is a hallmark of proficient, automatic word recognition. Previous research suggests that there is a delay before a new spoken word becomes engaged in this process, with sleep playing an important role. However, data from one method – the visual world paradigm – consistently show competition without a delay. We trained 42 adults and 40 children (aged 7–8) on novel word-object pair-ings, and employed this paradigm to measure the time-course of lexical competition. Fixations to novel objects upon hearing existing words (e.g., looks to the novel object biscal upon hearing ''click on the biscuit ") were compared to fixations on untrained objects. Novel word-object pairings learned immediately before testing and those learned the previous day exhibited significant competition effects, with stronger competition for the previous day pairings for children but not adults. Crucially, this competition effect was significantly smaller for novel than existing competitors (e.g., looks to candy upon hearing ''click on the candle "), suggesting that novel items may not compete for recognition like fully-fledged lexical items, even after 24 h. Explicit memory (cued recall) was superior for words learned the day before testing , particularly for children; this effect (but not the lexical competition effects) correlated with sleep-spindle density. Together, the results suggest that different aspects of new word learning follow different time courses: visual world competition effects can emerge swiftly, but are qualitatively different from those observed with established words, and are less reliant upon sleep. Furthermore, the findings fit with the view that word learning earlier in development is boosted by sleep to a greater degree.
Extracting regularities from a sequence of events is essential for understanding our environment.... more Extracting regularities from a sequence of events is essential for understanding our environment. However, there is no consensus regarding the extent to which such regularities can be generalised beyond the modality of learning. One reason for this could be the variation in consolidation intervals used in different paradigms, also including an opportunity to sleep. Using a novel statistical learning paradigm in which structured information is acquired in the auditory domain and tested in the visual domain over either 30 min or 24 h consolidation intervals, we show that cross-modal transfer can occur, but this transfer is only seen in the 24 h group. Importantly, the extent of cross-modal transfer is predicted by the amount of slow wave sleep (SWS) obtained. Additionally, cross-modal transfer is associated with the same pattern of decreasing medial temporal lobe and increasing striatal involvement which has previously been observed to occur across 24 h in unimodal statistical learning. We also observed enhanced functional connectivity after 24 h in a network of areas which have been implicated in cross-modal integration including the precuneus and the middle occipital gyrus. Finally, functional connectivity between the striatum and the precuneus was also enhanced, and this strengthening was predicted by SWS. These results demonstrate that statistical learning can generalise to some extent beyond the modality of acquisition, and together with our previously published unimodal results, support the notion that statistical learning is both domain-general and domain-specific.
Study Objectives: To investigate how the effects of targeted memory reactivation (TMR) are influe... more Study Objectives: To investigate how the effects of targeted memory reactivation (TMR) are influenced by memory accuracy prior to sleep and the presence or absence of direct cue-memory associations. Methods: 30 participants associated each of 50 pictures with an unrelated word and then with a screen location in two separate tasks. During picture-location training, each picture was also presented with a semantically related sound. The sounds were therefore directly associated with the picture locations but indirectly associated with the words. During a subsequent nap, half of the sounds were replayed in slow wave sleep (SWS). The effect of TMR on memory for the picture locations (direct cue-memory associations) and picture-word pairs (indirect cue-memory associations) was then examined. Results: TMR reduced overall memory decay for recall of picture locations. Further analyses revealed a benefit of TMR for picture locations recalled with a low degree of accuracy prior to sleep, but not those recalled with a high degree of accuracy. The benefit of TMR for low accuracy memories was predicted by time spent in SWS. There was no benefit of TMR for memory of the picture-word pairs, irrespective of memory accuracy prior to sleep. Conclusions: TMR provides the greatest benefit to memories recalled with a low degree of accuracy prior to sleep. The memory benefits of TMR may also be contingent on direct cue-memory associations.
Memory consolidation is most commonly described by the standard model, which proposes an initial ... more Memory consolidation is most commonly described by the standard model, which proposes an initial binding role for the hippocampus which diminishes over time as intracortical connections are strengthened. Recent evidence suggests that slow wave sleep (SWS) plays an essential role in this process. Existing animal and human studies have suggested that memories which fit tightly into an existing knowledge framework or schema might use an alternative consolidation route in which the medial prefrontal cortex takes on the binding role. In this study we sought to investigate the role of sleep in this process using a novel melodic memory task. Participants were asked to remember 32 melodies, half of which conformed to a tonal schema present in all enculturated listeners, and half of which did not fit with this schema. After a 24-h consolidation interval, participants were asked to remember a further 32 melodies, before being given a recognition test in which melodies from both sessions were presented alongside some previously unheard foils. Participants remembered schema-conformant melodies better than non-conformant ones. This was much more strongly the case for consolidated melodies, suggesting that consolidation over a 24-h period preferentially consolidated schema-conformant items. Overnight sleep was monitored between the sessions, and the extent of the consolidation benefit for schema-conformant items was associated with both the amount of REM sleep obtained and EEG theta power in frontal and central regions during REM sleep. Overall our data suggest that REM sleep plays a crucial role in the rapid consolidation of schema-conformant items. This finding is consistent with previous results from animal studies and the SLIMM model of Van Kesteren, Ruiter, Fernández, and Henson (2012), and suggest that REM sleep, rather than SWS, may be involved in an alternative pathway of consolidation for schema-conformant memories.
Emotional memories tend to be strengthened ahead of neutral memories during sleep-dependent conso... more Emotional memories tend to be strengthened ahead of neutral memories during sleep-dependent consolidation. In recent work, however, we found that this is not the case when emotion pertains to the contextual features of a memory instead of its central constructs, suggesting that emotional contexts are influenced by distinct properties of sleep. We therefore examined the sleep-specific mechanisms supporting representations of emotional context and asked whether these differ to those already implicated in central emotional memory processing, such as rapid eye movement sleep (REM). Participants encoded neutral foreground images that were each associated with an emotionally negative or neutral background (context) image. Immediate and delayed tests for the emotionality of the foreground/background image association were separated by a 4-h consolidation period, which consisted of either total wakefulness or included a 2-h polysomnographically monitored nap. Although memory for negative contexts was not associated with REM, or any other parameter of sleep, sleep spindles (12-15Hz) predicted increased forgetting and slowed response times for neutral contexts. Together with prior work linking spindles to emotional memory processing, our data may suggest that spindles provide multi-layered support to emotionally salient memories in sleep, with the nature of such effects depending on whether the emotionality of such memories pertains to their central or contextual features. Therefore, whereas spindles may mediate a direct strengthening of central emotional information, as suggested in prior work, they may also provide concurrent indirect support to emotional contexts by working to suppress non-salient neutral contexts.
STUDY OBJECTIVES
To investigate the mechanisms by which auditory targeted memory reactivation (T... more STUDY OBJECTIVES
To investigate the mechanisms by which auditory targeted memory reactivation (TMR) during slow wave sleep (SWS) influences the consolidation of emotionally negative and neutral memories.
DESIGN:
Each of 72 (36 negative, 36 neutral) picture-location associations were encoded with a semantically related sound. During a subsequent nap, half of the sounds were replayed in SWS, before picture-location recall was examined in a final test.
SETTING:
Manchester Sleep Laboratory, University of Manchester.
PARTICIPANTS:
15 adults (3 male) mean age = 20.40 (standard deviation ± 3.07).
INTERVENTIONS:
TMR with auditory cues during SWS.
MEASUREMENTS AND RESULTS:
Performance was assessed by memory accuracy and recall response times (RTs). Data were analyzed with a 2 (sound: replayed/not replayed) × 2 (emotion: negative/neutral) repeated measures analysis of covariance with SWS duration, and then SWS spindles, as the mean-centered covariate. Both analyses revealed a significant three-way interaction for RTs but not memory accuracy. Critically, SWS duration and SWS spindles predicted faster memory judgments for negative, relative to neutral, picture locations that were cued with TMR.
CONCLUSIONS:
TMR initiates an enhanced consolidation process during subsequent SWS, wherein sleep spindles mediate the selective enhancement of reactivated emotional memories.
CITATION:
Cairney SA; Durrant SJ; Hulleman J; Lewis PA. Targeted memory reactivation during slow wave sleep facilitates emotional memory consolidation. SLEEP 2014;37(4):701-707."
Although rapid eye movement sleep (REM) is regularly implicated in emotional memory consolidation... more Although rapid eye movement sleep (REM) is regularly implicated in emotional memory consolidation, the role of slow-wave sleep (SWS) in this process is largely uncharacterized. In the present study, we investigated the relative impacts of nocturnal SWS and REM upon the consolidation of emotional memories using functional magnetic resonance imaging (fMRI) and polysomnography (PSG). Participants encoded emotionally positive, negative, and neutral images (remote memories) before a night of PSG-monitored sleep. Twenty-four hours later, they encoded a second set of images (recent memories) immediately before a recognition test in an MRI scanner. SWS predicted superior memory for remote negative images and a reduction in right hippocampal responses during the recollection of these items. REM, however, predicted an overnight increase in hippocampal-neocortical connectivity associated with negative remote memory. These findings provide physiological support for sequential views of sleep-dependent memory processing, demonstrating that SWS and REM serve distinct but complementary functions in consolidation. Furthermore, these findings extend those ideas to emotional memory by showing that, once selectively reorganized away from the hippocampus during SWS, emotionally aversive representations undergo a comparably targeted process during subsequent REM.
Sleep after learning is often beneficial for memory. Reinstating an environmental context that wa... more Sleep after learning is often beneficial for memory. Reinstating an environmental context that was present at learning during subsequent retrieval also leads to superior declarative memory performance. This study examined how post-learning sleep, relative to wakefulness, impacts upon context-dependent memory effects. Thirty-two participants encoded word lists in each of two rooms (contexts), which were different in terms of size, odour and background music. Immediately after learning and following a night of sleep or a day of wakefulness, memory for all previously studied words was tested using a category-cued recall task in room one or two alone. Accordingly, a comparison could be made between words retrieved in an environmental context which was the same as, or different to, that of the learning phase. Memory performance was assessed by the difference between the number of words remembered at immediate and delayed retrieval. A 2 × 2 × 2 mixed ANOVA revealed an interaction between retrieval context (same/different to learning) and retention interval (sleep/wakefulness), which was driven by superior memory after sleep than after wake when learning and retrieval took place in different environmental contexts. Our findings suggest a sleep-related reduction in the extent to which context impacts upon retrieval. As such, these data provide initial support for the possibility that sleep dependent processes may promote a decontextualisation of recently formed declarative representations
Sleep is important for abstraction of the underlying principles (or gist) which bind together con... more Sleep is important for abstraction of the underlying principles (or gist) which bind together conceptually related stimuli, but little is known about the neural correlates of this process. Here, we investigate this issue using overnight sleep monitoring and functional magnetic resonance imaging (fMRI). Participants were exposed to a statistically structured sequence of auditory tones then tested immediately for recognition of short sequences which conformed to the learned statistical pattern. Subsequently, after consolidation over either 30 min or 24h, they performed a delayed test session in which brain activity was monitored with fMRI. Behaviorally, there was greater improvement across 24h than across 30 min, and this was predicted by the amount of slow wave sleep (SWS) obtained. Functionally, we observed weaker parahippocampal responses and stronger striatal responses after sleep. Like the behavioral result, these differences in functional response were predicted by the amount of SWS obtained. Furthermore, connectivity between striatum and parahippocampus was weaker after sleep, whereas connectivity between putamen and planum temporale was stronger. Taken together, these findings suggest that abstraction is associated with a gradual shift from the hippocampal to the striatal memory system and that this may be mediated by SWS
The importance of sleep for memory consolidation has been firmly established over the past decade... more The importance of sleep for memory consolidation has been firmly established over the past decade. Recent work has extended this by suggesting that sleep is also critical for the integration of disparate fragments of information into a unified schema, and for the abstraction of underlying rules. The question of which aspects of sleep play a significant role in integration and abstraction is, however, currently unresolved. Here, we examined the role of sleep in abstraction of the implicit probabilistic structure in sequential stimuli using a statistical learning paradigm, and tested for its role in such abstraction by searching for a predictive relationship between the type of sleep obtained and subsequent performance improvements using polysomnography. In our experiments, participants were exposed to a series of tones in a probabilistically determined sequential structure, and subsequently tested for recognition of novel short sequences adhering to this same statistical pattern in both immediate- and delayed-recall sessions. Participants who consolidated over a night of sleep improved significantly more than those who consolidated over an equivalent period of daytime wakefulness. Similarly, participants who consolidated across a 4-h afternoon delay containing a nap improved significantly more than those who consolidated across an equivalent period without a nap. Importantly, polysomnography revealed a significant correlation between the level of improvement and the amount of slow-wave sleep obtained. We also found evidence of a time-based consolidation process which operates alongside sleep-specific consolidation. These results demonstrate that abstraction of statistical patterns benefits from sleep, and provide the first clear support for the role of slow-wave sleep in this consolidation.
Sleep plays a role in the consolidation of declarative memories. Although this influence has attr... more Sleep plays a role in the consolidation of declarative memories. Although this influence has attracted much attention at the level of behavioural performance, few reports have searched for neural correlates. Here, we studied the impact of sleep upon memory for the context in which stimuli were learned at both behavioural and neural levels. Participants retrieved the association between a presented foreground object and its encoding context following a 12-h retention interval including either wake only or wake plus a night of sleep. Since sleep has been shown to selectively enhance some forms of emotional memory, we examined both neutral and emotionally valenced contexts. Behaviourally, less forgetting was observed across retention intervals containing sleep than retention intervals containing only wakefulness, and this benefit was accompanied by stronger responses in hippocampus and superior parietal cortex. This sleep-related reduction in forgetting did not differ between neutral and negative contexts, but there was a clear interaction between sleep and context valence at the functional level, with left amygdala, right parahippocampus, and other components of the episodic memory system all responding more strongly during correct memory for emotional contexts post-sleep. Connectivity between right parahippocampus and bilateral amygdala/periamygdala was also enhanced during correct post-sleep attribution of emotional contexts. Because there was no interaction between sleep and valence in terms of context memory performance these functional results may be associated with memory for details about the emotional encoding context rather than for the link between that context and the foreground object. Overall, our data show that while context memory decays less across sleep than across an equivalent period of wake, the sleep-related protection of such associations is not influenced by context emotionality in the same way as direct recollection of emotional information.
Retrieval facilitates the long-term retention of memories, but may also enable stored representat... more Retrieval facilitates the long-term retention of memories, but may also enable stored representations to be updated with new information that is available at the time of retrieval. However, if information integrated during retrieval is erroneous, future recall can be impaired: a phenomenon known as retrieval-induced distortion (RID). Whether RID causes an " overwriting " of existing memory traces or leads to the coexistence of original and distorted memory traces is unknown. Because sleep enhances memory consolidation, the effects of sleep after RID can provide novel insights into the structure of updated memories. As such, we investigated the effects of sleep on memory consolidation following RID. Participants encoded word locations and were then tested before (T1) and after (T2) an interval of sleep or wakefulness. At T2, the majority of words were placed closer to the locations retrieved at T1 than to the studied locations, consistent with RID. After sleep compared with after wake, the T2-retrieved locations were closer to both the studied locations and the T1-retrieved locations. These findings suggest that RID leads to the formation of an additional memory trace that corresponds to a distorted variant of the same encoding event, which is strengthened alongside the original trace during sleep. More broadly, these data provide evidence for the importance of sleep in the preservation and adaptive updating of memories.
Study Objectives: Memories are strengthened during sleep. The benefits of sleep for memory can be... more Study Objectives: Memories are strengthened during sleep. The benefits of sleep for memory can be enhanced by re-exposing the sleeping brain to auditory cues; a technique known as targeted memory reactivation (TMR). Prior studies have not assessed the nature of the retrieval mechanisms underpinning TMR: the matching process between auditory stimuli encountered during sleep and previously encoded memories. We carried out two experiments to address this issue. Methods: In Experiment 1, participants associated words with verbal and nonverbal auditory stimuli before an overnight interval in which subsets of these stimuli were replayed in slow-wave sleep. We repeated this paradigm in Experiment 2 with the single difference that the gender of the verbal auditory stimuli was switched between learning and sleep. Results: In Experiment 1, forgetting of cued (vs. noncued) associations was reduced by TMR with verbal and nonverbal cues to similar extents. In Experiment 2, TMR with identical nonverbal cues reduced forgetting of cued (vs. noncued) associations, replicating Experiment 1. However, TMR with nonidentical verbal cues reduced forgetting of both cued and noncued associations. Conclusions: These experiments suggest that the memory effects of TMR are influenced by the acoustic overlap between stimuli delivered at training and sleep. Our findings hint at the existence of two processing routes for memory retrieval during sleep. Whereas TMR with acoustically identical cues may reactivate individual associations via simple episodic matching, TMR with nonidentical verbal cues may utilize linguistic decoding mechanisms, resulting in widespread reactivation across a broad category of memories.
Recent work has suggested that the benefits of sleep for memory consolidation are enhanced for hi... more Recent work has suggested that the benefits of sleep for memory consolidation are enhanced for highly salient (versus non-salient) memories. Using a technique known as targeted memory reactivation, it is possible to selectively strengthen newly learned memories by re-exposing the sleeping brain to auditory cues. The aim of the current study was to examine whether emotionally salient memories are also more responsive to targeted memory reactivation in slow-wave sleep than neutral memories. In an initial training phase, participants memorised emotionally negative and neutral pictures, which were each paired with a semantically related sound. Recognition for the pictures was assessed before and after a 90-min nap opportunity, during which half the sounds were represented during slow-wave sleep (as assessed via online polysomnographic sleep monitoring). We observed no effect of targeted memory reactivation on the recognition of emotionally negative or neutral memories. Our results highlight the importance of the memory paradigm used to assess targeted memory reactivation, and suggest that the robust and durable nature of recognition memory may make it an insensitive measure of behavioural targeted memory reactivation benefits. To fully assess the impacts of targeted memory reactivation on emotional memory processing in sleep, future studies should adopt experimental paradigms that maximise the salience of emotional stimuli while also providing a sensitive index of memory accuracy.
New memories are rarely formed as individual representations, but are stored in the context of co... more New memories are rarely formed as individual representations, but are stored in the context of cognitive schemas: mental frameworks within which we can organize and interpret related information (Bartlett, 1932). At school, for example, we acquire basic knowledge about the locations of different countries. This geographical schema then assists us later in life when learning about new countries, their locations, and cultural similarities. As our global knowledge grows, the learning and integration of new geographical information becomes increasingly efficient, and we can make inferences regarding the world around us. Schematic influences on learning can be understood in the context of dual systems models of memory (e.g., van Kesteren et al., 2012; McClelland, 2013). These models propose that new information is rapidly encoded by hippocampal networks, but becomes gradually integrated into the neocortex for long-term storage. However, where this new information is related to a schema, it benefits from existing neural connections and can thus be integrated more efficiently than unrelated information. Several recent studies have examined the neural mechanisms underlying schematic learning by generating artificial schema in the laboratory (e.g., Hennies et al., 2016). While informative and well-controlled, this method is unable to address how we utilize real-world knowledge that is not bound to the context of an experiment. Understanding whether the neural mechanisms underpinning schema-based learning are similar in relation to natural variations in existing knowledge remains a key research question. Gaining insights into the automaticity with which we can capitalize upon our existing knowledge in different settings from which it is acquired may have important implications for education. In a recent study, Brod et al. (2016) capitalized upon the advancing knowledge of medical students to gain more naturalistic insights into the neural basis of schema-relevant learning. While undergoing fMRI, participants learned a series of faces paired with either names or medical diagnoses (low or high relevance to medical knowledge, respectively). Immediately afterwards, outside of the scanner, they were represented with each face and asked to identify the associated name/diagnosis. This procedure enabled Brod et al. to identify patterns of neural activity at learning that predicted successful memory retrieval at test. Furthermore, this procedure was carried out with novel pairs both before and after 3 months of study for a medical exam, providing a measurable
Lexical competition is a hallmark of proficient, automatic word recognition. Previous research su... more Lexical competition is a hallmark of proficient, automatic word recognition. Previous research suggests that there is a delay before a new spoken word becomes engaged in this process, with sleep playing an important role. However, data from one method – the visual world paradigm – consistently show competition without a delay. We trained 42 adults and 40 children (aged 7–8) on novel word-object pair-ings, and employed this paradigm to measure the time-course of lexical competition. Fixations to novel objects upon hearing existing words (e.g., looks to the novel object biscal upon hearing ''click on the biscuit ") were compared to fixations on untrained objects. Novel word-object pairings learned immediately before testing and those learned the previous day exhibited significant competition effects, with stronger competition for the previous day pairings for children but not adults. Crucially, this competition effect was significantly smaller for novel than existing competitors (e.g., looks to candy upon hearing ''click on the candle "), suggesting that novel items may not compete for recognition like fully-fledged lexical items, even after 24 h. Explicit memory (cued recall) was superior for words learned the day before testing , particularly for children; this effect (but not the lexical competition effects) correlated with sleep-spindle density. Together, the results suggest that different aspects of new word learning follow different time courses: visual world competition effects can emerge swiftly, but are qualitatively different from those observed with established words, and are less reliant upon sleep. Furthermore, the findings fit with the view that word learning earlier in development is boosted by sleep to a greater degree.
Extracting regularities from a sequence of events is essential for understanding our environment.... more Extracting regularities from a sequence of events is essential for understanding our environment. However, there is no consensus regarding the extent to which such regularities can be generalised beyond the modality of learning. One reason for this could be the variation in consolidation intervals used in different paradigms, also including an opportunity to sleep. Using a novel statistical learning paradigm in which structured information is acquired in the auditory domain and tested in the visual domain over either 30 min or 24 h consolidation intervals, we show that cross-modal transfer can occur, but this transfer is only seen in the 24 h group. Importantly, the extent of cross-modal transfer is predicted by the amount of slow wave sleep (SWS) obtained. Additionally, cross-modal transfer is associated with the same pattern of decreasing medial temporal lobe and increasing striatal involvement which has previously been observed to occur across 24 h in unimodal statistical learning. We also observed enhanced functional connectivity after 24 h in a network of areas which have been implicated in cross-modal integration including the precuneus and the middle occipital gyrus. Finally, functional connectivity between the striatum and the precuneus was also enhanced, and this strengthening was predicted by SWS. These results demonstrate that statistical learning can generalise to some extent beyond the modality of acquisition, and together with our previously published unimodal results, support the notion that statistical learning is both domain-general and domain-specific.
Study Objectives: To investigate how the effects of targeted memory reactivation (TMR) are influe... more Study Objectives: To investigate how the effects of targeted memory reactivation (TMR) are influenced by memory accuracy prior to sleep and the presence or absence of direct cue-memory associations. Methods: 30 participants associated each of 50 pictures with an unrelated word and then with a screen location in two separate tasks. During picture-location training, each picture was also presented with a semantically related sound. The sounds were therefore directly associated with the picture locations but indirectly associated with the words. During a subsequent nap, half of the sounds were replayed in slow wave sleep (SWS). The effect of TMR on memory for the picture locations (direct cue-memory associations) and picture-word pairs (indirect cue-memory associations) was then examined. Results: TMR reduced overall memory decay for recall of picture locations. Further analyses revealed a benefit of TMR for picture locations recalled with a low degree of accuracy prior to sleep, but not those recalled with a high degree of accuracy. The benefit of TMR for low accuracy memories was predicted by time spent in SWS. There was no benefit of TMR for memory of the picture-word pairs, irrespective of memory accuracy prior to sleep. Conclusions: TMR provides the greatest benefit to memories recalled with a low degree of accuracy prior to sleep. The memory benefits of TMR may also be contingent on direct cue-memory associations.
Memory consolidation is most commonly described by the standard model, which proposes an initial ... more Memory consolidation is most commonly described by the standard model, which proposes an initial binding role for the hippocampus which diminishes over time as intracortical connections are strengthened. Recent evidence suggests that slow wave sleep (SWS) plays an essential role in this process. Existing animal and human studies have suggested that memories which fit tightly into an existing knowledge framework or schema might use an alternative consolidation route in which the medial prefrontal cortex takes on the binding role. In this study we sought to investigate the role of sleep in this process using a novel melodic memory task. Participants were asked to remember 32 melodies, half of which conformed to a tonal schema present in all enculturated listeners, and half of which did not fit with this schema. After a 24-h consolidation interval, participants were asked to remember a further 32 melodies, before being given a recognition test in which melodies from both sessions were presented alongside some previously unheard foils. Participants remembered schema-conformant melodies better than non-conformant ones. This was much more strongly the case for consolidated melodies, suggesting that consolidation over a 24-h period preferentially consolidated schema-conformant items. Overnight sleep was monitored between the sessions, and the extent of the consolidation benefit for schema-conformant items was associated with both the amount of REM sleep obtained and EEG theta power in frontal and central regions during REM sleep. Overall our data suggest that REM sleep plays a crucial role in the rapid consolidation of schema-conformant items. This finding is consistent with previous results from animal studies and the SLIMM model of Van Kesteren, Ruiter, Fernández, and Henson (2012), and suggest that REM sleep, rather than SWS, may be involved in an alternative pathway of consolidation for schema-conformant memories.
Emotional memories tend to be strengthened ahead of neutral memories during sleep-dependent conso... more Emotional memories tend to be strengthened ahead of neutral memories during sleep-dependent consolidation. In recent work, however, we found that this is not the case when emotion pertains to the contextual features of a memory instead of its central constructs, suggesting that emotional contexts are influenced by distinct properties of sleep. We therefore examined the sleep-specific mechanisms supporting representations of emotional context and asked whether these differ to those already implicated in central emotional memory processing, such as rapid eye movement sleep (REM). Participants encoded neutral foreground images that were each associated with an emotionally negative or neutral background (context) image. Immediate and delayed tests for the emotionality of the foreground/background image association were separated by a 4-h consolidation period, which consisted of either total wakefulness or included a 2-h polysomnographically monitored nap. Although memory for negative contexts was not associated with REM, or any other parameter of sleep, sleep spindles (12-15Hz) predicted increased forgetting and slowed response times for neutral contexts. Together with prior work linking spindles to emotional memory processing, our data may suggest that spindles provide multi-layered support to emotionally salient memories in sleep, with the nature of such effects depending on whether the emotionality of such memories pertains to their central or contextual features. Therefore, whereas spindles may mediate a direct strengthening of central emotional information, as suggested in prior work, they may also provide concurrent indirect support to emotional contexts by working to suppress non-salient neutral contexts.
STUDY OBJECTIVES
To investigate the mechanisms by which auditory targeted memory reactivation (T... more STUDY OBJECTIVES
To investigate the mechanisms by which auditory targeted memory reactivation (TMR) during slow wave sleep (SWS) influences the consolidation of emotionally negative and neutral memories.
DESIGN:
Each of 72 (36 negative, 36 neutral) picture-location associations were encoded with a semantically related sound. During a subsequent nap, half of the sounds were replayed in SWS, before picture-location recall was examined in a final test.
SETTING:
Manchester Sleep Laboratory, University of Manchester.
PARTICIPANTS:
15 adults (3 male) mean age = 20.40 (standard deviation ± 3.07).
INTERVENTIONS:
TMR with auditory cues during SWS.
MEASUREMENTS AND RESULTS:
Performance was assessed by memory accuracy and recall response times (RTs). Data were analyzed with a 2 (sound: replayed/not replayed) × 2 (emotion: negative/neutral) repeated measures analysis of covariance with SWS duration, and then SWS spindles, as the mean-centered covariate. Both analyses revealed a significant three-way interaction for RTs but not memory accuracy. Critically, SWS duration and SWS spindles predicted faster memory judgments for negative, relative to neutral, picture locations that were cued with TMR.
CONCLUSIONS:
TMR initiates an enhanced consolidation process during subsequent SWS, wherein sleep spindles mediate the selective enhancement of reactivated emotional memories.
CITATION:
Cairney SA; Durrant SJ; Hulleman J; Lewis PA. Targeted memory reactivation during slow wave sleep facilitates emotional memory consolidation. SLEEP 2014;37(4):701-707."
Although rapid eye movement sleep (REM) is regularly implicated in emotional memory consolidation... more Although rapid eye movement sleep (REM) is regularly implicated in emotional memory consolidation, the role of slow-wave sleep (SWS) in this process is largely uncharacterized. In the present study, we investigated the relative impacts of nocturnal SWS and REM upon the consolidation of emotional memories using functional magnetic resonance imaging (fMRI) and polysomnography (PSG). Participants encoded emotionally positive, negative, and neutral images (remote memories) before a night of PSG-monitored sleep. Twenty-four hours later, they encoded a second set of images (recent memories) immediately before a recognition test in an MRI scanner. SWS predicted superior memory for remote negative images and a reduction in right hippocampal responses during the recollection of these items. REM, however, predicted an overnight increase in hippocampal-neocortical connectivity associated with negative remote memory. These findings provide physiological support for sequential views of sleep-dependent memory processing, demonstrating that SWS and REM serve distinct but complementary functions in consolidation. Furthermore, these findings extend those ideas to emotional memory by showing that, once selectively reorganized away from the hippocampus during SWS, emotionally aversive representations undergo a comparably targeted process during subsequent REM.
Sleep after learning is often beneficial for memory. Reinstating an environmental context that wa... more Sleep after learning is often beneficial for memory. Reinstating an environmental context that was present at learning during subsequent retrieval also leads to superior declarative memory performance. This study examined how post-learning sleep, relative to wakefulness, impacts upon context-dependent memory effects. Thirty-two participants encoded word lists in each of two rooms (contexts), which were different in terms of size, odour and background music. Immediately after learning and following a night of sleep or a day of wakefulness, memory for all previously studied words was tested using a category-cued recall task in room one or two alone. Accordingly, a comparison could be made between words retrieved in an environmental context which was the same as, or different to, that of the learning phase. Memory performance was assessed by the difference between the number of words remembered at immediate and delayed retrieval. A 2 × 2 × 2 mixed ANOVA revealed an interaction between retrieval context (same/different to learning) and retention interval (sleep/wakefulness), which was driven by superior memory after sleep than after wake when learning and retrieval took place in different environmental contexts. Our findings suggest a sleep-related reduction in the extent to which context impacts upon retrieval. As such, these data provide initial support for the possibility that sleep dependent processes may promote a decontextualisation of recently formed declarative representations
Sleep is important for abstraction of the underlying principles (or gist) which bind together con... more Sleep is important for abstraction of the underlying principles (or gist) which bind together conceptually related stimuli, but little is known about the neural correlates of this process. Here, we investigate this issue using overnight sleep monitoring and functional magnetic resonance imaging (fMRI). Participants were exposed to a statistically structured sequence of auditory tones then tested immediately for recognition of short sequences which conformed to the learned statistical pattern. Subsequently, after consolidation over either 30 min or 24h, they performed a delayed test session in which brain activity was monitored with fMRI. Behaviorally, there was greater improvement across 24h than across 30 min, and this was predicted by the amount of slow wave sleep (SWS) obtained. Functionally, we observed weaker parahippocampal responses and stronger striatal responses after sleep. Like the behavioral result, these differences in functional response were predicted by the amount of SWS obtained. Furthermore, connectivity between striatum and parahippocampus was weaker after sleep, whereas connectivity between putamen and planum temporale was stronger. Taken together, these findings suggest that abstraction is associated with a gradual shift from the hippocampal to the striatal memory system and that this may be mediated by SWS
The importance of sleep for memory consolidation has been firmly established over the past decade... more The importance of sleep for memory consolidation has been firmly established over the past decade. Recent work has extended this by suggesting that sleep is also critical for the integration of disparate fragments of information into a unified schema, and for the abstraction of underlying rules. The question of which aspects of sleep play a significant role in integration and abstraction is, however, currently unresolved. Here, we examined the role of sleep in abstraction of the implicit probabilistic structure in sequential stimuli using a statistical learning paradigm, and tested for its role in such abstraction by searching for a predictive relationship between the type of sleep obtained and subsequent performance improvements using polysomnography. In our experiments, participants were exposed to a series of tones in a probabilistically determined sequential structure, and subsequently tested for recognition of novel short sequences adhering to this same statistical pattern in both immediate- and delayed-recall sessions. Participants who consolidated over a night of sleep improved significantly more than those who consolidated over an equivalent period of daytime wakefulness. Similarly, participants who consolidated across a 4-h afternoon delay containing a nap improved significantly more than those who consolidated across an equivalent period without a nap. Importantly, polysomnography revealed a significant correlation between the level of improvement and the amount of slow-wave sleep obtained. We also found evidence of a time-based consolidation process which operates alongside sleep-specific consolidation. These results demonstrate that abstraction of statistical patterns benefits from sleep, and provide the first clear support for the role of slow-wave sleep in this consolidation.
Sleep plays a role in the consolidation of declarative memories. Although this influence has attr... more Sleep plays a role in the consolidation of declarative memories. Although this influence has attracted much attention at the level of behavioural performance, few reports have searched for neural correlates. Here, we studied the impact of sleep upon memory for the context in which stimuli were learned at both behavioural and neural levels. Participants retrieved the association between a presented foreground object and its encoding context following a 12-h retention interval including either wake only or wake plus a night of sleep. Since sleep has been shown to selectively enhance some forms of emotional memory, we examined both neutral and emotionally valenced contexts. Behaviourally, less forgetting was observed across retention intervals containing sleep than retention intervals containing only wakefulness, and this benefit was accompanied by stronger responses in hippocampus and superior parietal cortex. This sleep-related reduction in forgetting did not differ between neutral and negative contexts, but there was a clear interaction between sleep and context valence at the functional level, with left amygdala, right parahippocampus, and other components of the episodic memory system all responding more strongly during correct memory for emotional contexts post-sleep. Connectivity between right parahippocampus and bilateral amygdala/periamygdala was also enhanced during correct post-sleep attribution of emotional contexts. Because there was no interaction between sleep and valence in terms of context memory performance these functional results may be associated with memory for details about the emotional encoding context rather than for the link between that context and the foreground object. Overall, our data show that while context memory decays less across sleep than across an equivalent period of wake, the sleep-related protection of such associations is not influenced by context emotionality in the same way as direct recollection of emotional information.
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Papers by Scott Cairney
To investigate the mechanisms by which auditory targeted memory reactivation (TMR) during slow wave sleep (SWS) influences the consolidation of emotionally negative and neutral memories.
DESIGN:
Each of 72 (36 negative, 36 neutral) picture-location associations were encoded with a semantically related sound. During a subsequent nap, half of the sounds were replayed in SWS, before picture-location recall was examined in a final test.
SETTING:
Manchester Sleep Laboratory, University of Manchester.
PARTICIPANTS:
15 adults (3 male) mean age = 20.40 (standard deviation ± 3.07).
INTERVENTIONS:
TMR with auditory cues during SWS.
MEASUREMENTS AND RESULTS:
Performance was assessed by memory accuracy and recall response times (RTs). Data were analyzed with a 2 (sound: replayed/not replayed) × 2 (emotion: negative/neutral) repeated measures analysis of covariance with SWS duration, and then SWS spindles, as the mean-centered covariate. Both analyses revealed a significant three-way interaction for RTs but not memory accuracy. Critically, SWS duration and SWS spindles predicted faster memory judgments for negative, relative to neutral, picture locations that were cued with TMR.
CONCLUSIONS:
TMR initiates an enhanced consolidation process during subsequent SWS, wherein sleep spindles mediate the selective enhancement of reactivated emotional memories.
CITATION:
Cairney SA; Durrant SJ; Hulleman J; Lewis PA. Targeted memory reactivation during slow wave sleep facilitates emotional memory consolidation. SLEEP 2014;37(4):701-707."
To investigate the mechanisms by which auditory targeted memory reactivation (TMR) during slow wave sleep (SWS) influences the consolidation of emotionally negative and neutral memories.
DESIGN:
Each of 72 (36 negative, 36 neutral) picture-location associations were encoded with a semantically related sound. During a subsequent nap, half of the sounds were replayed in SWS, before picture-location recall was examined in a final test.
SETTING:
Manchester Sleep Laboratory, University of Manchester.
PARTICIPANTS:
15 adults (3 male) mean age = 20.40 (standard deviation ± 3.07).
INTERVENTIONS:
TMR with auditory cues during SWS.
MEASUREMENTS AND RESULTS:
Performance was assessed by memory accuracy and recall response times (RTs). Data were analyzed with a 2 (sound: replayed/not replayed) × 2 (emotion: negative/neutral) repeated measures analysis of covariance with SWS duration, and then SWS spindles, as the mean-centered covariate. Both analyses revealed a significant three-way interaction for RTs but not memory accuracy. Critically, SWS duration and SWS spindles predicted faster memory judgments for negative, relative to neutral, picture locations that were cued with TMR.
CONCLUSIONS:
TMR initiates an enhanced consolidation process during subsequent SWS, wherein sleep spindles mediate the selective enhancement of reactivated emotional memories.
CITATION:
Cairney SA; Durrant SJ; Hulleman J; Lewis PA. Targeted memory reactivation during slow wave sleep facilitates emotional memory consolidation. SLEEP 2014;37(4):701-707."